insects Review A Review of Effects of Environment on Brain Size in Insects Thomas Carle Faculty of Biology, Kyushu University, Fukuoka 819-0395, Japan; [email protected] Simple Summary: What makes a big brain is fascinating since it is considered as a measure of intelligence. Above all, brain size is associated with body size. If species that have evolved with complex social behaviours possess relatively bigger brains than those deprived of such behaviours, this does not constitute the only factor affecting brain size. Other factors such as individual experience or surrounding environment also play roles in the size of the brain. In this review, I summarize the recent findings about the effects of environment on brain size in insects. I also discuss evidence about how the environment has an impact on sensory systems and influences brain size. Abstract: Brain size fascinates society as well as researchers since it is a measure often associated with intelligence and was used to define species with high “intellectual capabilities”. In general, brain size is correlated with body size. However, there are disparities in terms of relative brain size between species that may be explained by several factors such as the complexity of social behaviour, the ‘social brain hypothesis’, or learning and memory capabilities. These disparities are used to classify species according to an ‘encephalization quotient’. However, environment also has an important role on the development and evolution of brain size. In this review, I summarise the recent studies looking at the effects of environment on brain size in insects, and introduce the idea that the role of environment might be mediated through the relationship between olfaction and vision. I also discussed this idea with studies that contradict this way of thinking. Citation: Carle, T. A Review of Effects Keywords: brain size; environment; evolution of Environment on Brain Size in Insects. Insects 2021, 12, 461. https:// doi.org/10.3390/insects12050461 1. Introduction Academic Editors: Aya Yanagawa Brain is in perpetual change, through evolution between and within species or even and Mamiko Ozaki through the life of individuals. These changes do not only comprise specific neuronal structures that play specific functions (e.g., visual cortex, thalamus ... ) and are specific to Received: 11 February 2021 species, but also changes in neuronal networks and mechanisms. As a better comprehension Accepted: 12 May 2021 Published: 17 May 2021 of brain is fundamental in various domains such as evolutionary biology, psychology or ethology, to study brain has fascinated many researchers. In particular, researchers have been fascinated by its size since it could have been used to compare the level of intelligence Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in between species or individuals. In this review, I will brush off this idea by resuming studies published maps and institutional affil- investigating effects of environment on brain size in insects. iations. 2. Brain Size What makes a brain big? The idea that a bigger brain is directly related to better intelligence is biased on the fact that people naively and simply associate a bigger brain with a larger number of neurons and, therefore, a greater number of neural connexions. Copyright: © 2021 by the author. Licensee MDPI, Basel, Switzerland. However, many factors nullify this simplistic point of view, such as the size of neurons [1]. This article is an open access article Before talking about intelligence, Jerison [2] showed a general allometric relationship distributed under the terms and between brain size and body size across mammals. In other words, it means that brain conditions of the Creative Commons size is primarily dependant to body size, and was first found to follow the equation: Attribution (CC BY) license (https:// log (Brain weight) = 0.76 × log (Body weight) −1.28 [3,4], or more recently (50 years creativecommons.org/licenses/by/ later and using substantially more species) log (Brain weight) = 0.75 × log (Body weight) 4.0/). −1.26 [5]. Looking more attentively at Jerison’s study [2], there are disparities in this linear Insects 2021, 12, 461. https://doi.org/10.3390/insects12050461 https://www.mdpi.com/journal/insects Insects 2021, 12, 461 2 of 14 relationship between the logarithmic values of brain and body sizes between and within species: some species have a relative brain size larger than other species. In addition, when analysing this relationship between brain and body size by animal orders, the slope varies ranging from 0.24 to 0.81 [5]. These deviations have sometimes been used to estimate an animal’s cognitive abilities in comparison to other species. For example, the presence or absence of complex cognitive capabilities, which might be required in social behaviours, can affect brain size as posited by the ‘social brain hypothesis’ [6–11]. This idea persisted until recent studies suggested that ecological drivers, including diets, are better predictors of brain size than sociality in primates [12,13] and insects [14]. More generally, apart from ecological factors [15], other hypotheses considering energetic [16], life history [17] and behavioural factors [18] have been highlighted to explain these disparities and to support anticipated criticisms about the relation between brain size and intelligence [19–22]. The purpose of this review is not to question brain size due to the evolution of cognitive capabilities such as those involved in social behaviour or learning and memory capabilities, but to highlight the idea that environment also plays a role in evolution and development of brain size through a summary of studies done in insects and a parallel with mammals. 3. Haller’s Rule, Brain Size in Insects In 1762, A. von Haller predicted that smaller animals have relatively larger brains than larger-bodied forms, a concept known as ‘Haller’s rule’ [23]. This prediction is easily verifiable by the value of the slope that Armstrong [3,4] and Burger et al. [5] found in their equation. The slope being inferior to 1 means that the increase in brain weight is inferior to the increase in body weight during brain evolution and, as a result, smaller species possess relatively bigger brains. To take a concrete example, the brain takes a large portion of the body mass in insects, about 16% [24,25], whereas it takes about 2–2.5% of body mass in humans [26,27] and about 0.07–0.18% in elephants [28,29]. However, the brain–body mass ratio in adult mice is close to 1–1.6% [30,31], which is inferior to that seen in humans and seems to contradict Haller’s rule at first sight. This may be explained if humans are considered to be relatively more intelligent than mice. To take this argument further, we need to consider if ‘intelligence’ can be anatomically measured. To find a comparative anatomical measure of “intelligence” between species, Jerison and Barlow [32] proposed the ‘encephalization quotient’ (EQ): the ratio between brain mass observed and that predicted from body size within an animal of a given species. The EQ has been evaluated to equal 7.4–7.8 in humans, 1.3 in African elephants and 0.5 in mice [28]. This means that the human brain is 7–8 times larger than expected, whereas in mice, it is 0.5 times larger (or twice smaller) than expected. This may explain why elephants have a comparatively small brain–body ratio despite being considered as quite intelligent animals. It also shows that the human brain is disproportionally bigger compared to other species and explains why its relative size is superior to that in mice. However, the link between EQ and “intelligence” is still in debate [28], and recent ways of thinking tend to consider the number of neurons rather than the mass as a better indicator of cognitive capabilities see [33]. In general, insect brain size follows Haller’s rule (Figure1). This relationship is verifiable both between species [25,26,34], and within species [24,26,34,35]. However, recent studies have pointed to several exceptions to Haller’s rule [36,37]. For example, Van der Woude et al. [37] performed an intraspecific comparison between differently sized individuals of the small parasitic wasp Trichogramma evanescens, and showed for the first time an isometric brain–body size relation, so brain size is directly proportional to body size (with the brain occupying 8.2% of the body in this case). The authors explained their observations by the fact that an increase in expensive brain tissue in the smallest individuals would be too costly in terms of energy expenditure and, therefore, there would be a selective pressure for maintaining smaller brains in smaller individuals. In the line of Insects 2021, 12, x FOR PEER REVIEW 3 of 14 would be too costly in terms of energy expenditure and, therefore, there would be a selec‐ Insects 2021 12 , , 461 tive pressure for maintaining smaller brains in smaller individuals.3 of 14 In the line of this study, Groothius et al. [36] made the same observation in the wasp Nasonia vitripennis. However, in this case, the authors observed an isometric relationship for the smallest this study, Groothius et al. [36] made the same observation in the wasp Nasonia vitripennis. However,wasps, in thisbut case, not theon authors the largest observed individuals. an isometric relationship To date, these for the smallesttwo studies wasps, provide the only butexceptions not on the largest to Haller’s individuals. rule, To which date, thesemight two be studies associated provide with the onlythese exceptions wasps’ parasitic lifestyle. to Haller’s rule, which might be associated with these wasps’ parasitic lifestyle. Figure 1. Illustrations of brains across insects’ phylogeny. Figure 1. Illustrations of brains across insects’ phylogeny.